In vivo effects of 17β-estradiol on cardiac Na+/K+-ATPase expression and activity in rat heart

Molecular and Cellular Endocrinology

Volumn 388, Issue 1-2, 2014, Pages 58-68

  Obradovic, Milan ^a   Stewart, Alan J ^b   Pitt, Samantha J ^b   Labudovic Borovic, Milica ^c   Sudar, Emina ^a   Petrovic, Voin ^a   Zafirovic, Sonja ^a   Maravic Stojkovic, Vera ^d   Vasic, Vesna ^a   Isenovic, Esma R ^a  

^a UNIVERSITY OF BELGRADE   (Serbia)

^b UNIVERSITY OF ST ANDREWS   (United Kingdom)

^c UNIVERSITY OF BELGRADE   (Serbia)

^d Institute for Cardiovascular Diseases Dedinje   (Serbia)

Author keywords

Estradiol; Extracellular signal regulated kinase 1 2; Protein kinase B; Sodium potassium adenosine triphosphatase

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM) SUBUNIT ALPHA 1; CHOLESTEROL; DIGITALIS LIKE FACTOR; ESTRADIOL; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MYC PROTEIN; POTASSIUM ION; PROTEIN C JUN; PROTEIN KINASE B; SODIUM ION; UNCLASSIFIED DRUG; CARDENOLIDE; DIGOXIN-LIKE FACTORS; MITOGEN ACTIVATED PROTEIN KINASE; SAPONIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARDIOVASCULAR EFFECT; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME PHOSPHORYLATION; ESTRADIOL BLOOD LEVEL; HORMONAL REGULATION; HORMONE ACTION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; ANIMAL; BLOOD; CELL MEMBRANE; ENZYMOLOGY; GENE EXPRESSION; GENETICS; HEART MUSCLE; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; WISTAR RAT;

ANIMALS; CARDENOLIDES; CELL MEMBRANE; CHOLESTEROL; ESTRADIOL; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION; MALE; MYOCARDIUM; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-JUN; PROTO-ONCOGENE PROTEINS C-MYC; RATS, WISTAR; SAPONINS; SIGNAL TRANSDUCTION; SODIUM-POTASSIUM-EXCHANGING ATPASE;

EID: 84897483356     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2014.03.005     Document Type: Article

References (103)

1. Aizman O., Uhlen P., Lal M., Brismar H., Aperia A. Ouabain, a steroid hormone that signals with slow calcium oscillations. Proc. Natl. Acad. Sci. USA 2001, 98(23):13420-13424.
2. Alessi D.R., Cohen P. Mechanism of activation and function of protein kinase B. Curr. Opin. Genet. Dev. 1998, 8(1):55-62.
3. +-ATPase trafficking in skeletal muscle: insulin stimulates translocation of both alpha 1- and alpha 2-subunit isoforms. FEBS Lett. 2003, 536(1-3):198-202.
4. Al-Khalili L., Kotova O., Tsuchida H., Ehren I., Feraille E., Krook A., Chibalin A.V. ERK1/2 mediates insulin stimulation of Na(+), K(+)-ATPase by phosphorylation of the alpha-subunit in human skeletal muscle cells. J. Biol. Chem. 2004, 279(24):25211-25218.
5. Aperia A. New roles for an old enzyme: Na, K-ATPase emerges as an interesting drug target. J. Intern. Med. 2007, 261(1):44-52.
6. Bagrov A.Y., Shapiro J.I., Fedorova O.V. Endogenous cardiotonic steroids: physiology, pharmacology, and novel therapeutic targets. Pharmacol. Rev. 2009, 61(1):9-38.
7. Barbacanne M.A., Rami J., Michel J.B., Souchard J.P., Philippe M., Besombes J.P., Bayard F., Arnal J.F. Estradiol increases rat aorta endothelium-derived relaxing factor (EDRF) activity without changes in endothelial NO syntheses gene expression: possible role of decreased endothelium-derived superoxide anion production. Cardiovasc. Res. 1999, 41(3):672-681.
8. Barros R.P., Gustafsson J.A. Estrogen receptors and the metabolic network. Cell Metab. 2011, 14(3):289-299.
9. Blalock W.L., Navolanic P.M., Steelman L.S., Shelton J.G., Moye P.W., Lee J.T., Franklin R.A., Mirza A., McMahon M., White M.K., et al. Requirement for the PI3K/Akt pathway in MEK1-mediated growth and prevention of apoptosis: identification of an Achilles heel in leukemia. Leukemia 2003, 17(6):1058-1067.
10. Burnette W.N. Western blotting: electrophoretic transfer of proteins from sodium dodecyl sulfate-polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal. Biochem. 1981, 112(2):195-203.
11. Campbell M., Allen W.E., Sawyer C., Vanhaesebroeck B., Trimble E.R. Glucose-potentiated chemotaxis in human vascular smooth muscle is dependent on cross-talk between the PI3K and MAPK signaling pathways. Circ. Res. 2004, 95(4):380-388.
12. Camper-Kirby D., Welch S., Walker A., Shiraishi I., Setchell K.D., Schaefer E., Kajstura J., Anversa P., Sussman M.A. Myocardial Akt activation and gender: increased nuclear activity in females versus males. Circ. Res. 2001, 88(10):1020-1027.
13. +-ATPase endocytosis. J. Biol. Chem. 1998, 273(15):8814-8819.
14. +-ATPase is initiated by phosphorylation of Ser-18 in the rat alpha subunit and Is responsible for the decreased activity in epithelial cells. J. Biol. Chem. 1999, 274(4):1920-1927.
15. Choukroun G., Hajjar R., Fry S., del Monte F., Haq S., Guerrero J.L., Picard M., Rosenzweig A., Force T. Regulation of cardiac hypertrophy in vivo by the stress-activated protein kinases/c-Jun NH(2)-terminal kinases. J Clin Invest. 1999, 104(4):391-398.
16. Deschamps A.M., Murphy E. Activation of a novel estrogen receptor, GPER, is cardioprotective in male and female rats. Am. J. Physiol. Heart Circ. Physiol. 2009, 297(5):H1806-H1813.
17. Dzurba A., Ziegelhoffer A., Vrbjar N., Styk J., Slezak J. Estradiol modulates the sodium pump in the heart sarcolemma. Mol. Cell. Biochem. 1997, 176(1-2):113-118.
18. Efendiev R., Das-Panja K., Cinelli A.R., Bertorello A.M., Pedemonte C.H. Localization of intracellular compartments that exchange Na, K-ATPase molecules with the plasma membrane in a hormone-dependent manner. Br. J. Pharmacol. 2007, 151(7):1006-1013.
19. Ewart H.S., Klip A. Hormonal regulation of the Na(+)-K(+)-ATPase: mechanisms underlying rapid and sustained changes in pump activity. Am. J. Physiol. 1995, 269(2 Pt 1):C295-C311.
20. Fuller W., Tulloch L.B., Shattock M.J., Calaghan S.C., Howie J., Wypijewski K.J. Regulation of the cardiac sodium pump. Cell. Mol. Life Sci. 2013, 70(8):1357-1380.
21. Gardner J.D., Murray D.B., Voloshenyuk T.G., Brower G.L., Bradley J.M., Janicki J.S. Estrogen attenuates chronic volume overload induced structural and functional remodeling in male rat hearts. Am. J. Physiol. Heart Circ. Physiol. 2010, 298(2):H497-H504.
22. Gheorghiade M., Hall V.B., Jacobsen G., Alam M., Rosman H., Goldstein S. Effects of increasing maintenance dose of digoxin on left ventricular function and neurohormones in patients with chronic heart failure treated with diuretics and angiotensin-converting enzyme inhibitors. Circulation 1995, 92(7):1801-1807.
23. +-ATPase expression in the renal cortex. Cell. Physiol. Biochem. 2012, 30(1):160-172.
24. Grohe C., Kahlert S., Lobbert K., Vetter H. Expression of oestrogen receptor alpha and beta in rat heart: role of local oestrogen synthesis. J. Endocrinol. 1998, 156(2):R1-R7.
25. Group TDI The effect of digoxin on mortality and morbidity in patients with heart failure. The Digitalis Investigation Group. N. Engl. J. Med. 1997, 336(8):525-533.
26. Handgraaf S., Riant E., Fabre A., Waget A., Burcelin R., Liere P., Krust A., Chambon P., Arnal J.F., Gourdy P. Prevention of obesity and insulin resistance by estrogens requires ERalpha activation function-2 (ERalphaAF-2), whereas ERalphaAF-1 is dispensable. Diabetes 2013.
27. Hao L., Wang Y., Duan Y., Bu S. Effects of treadmill exercise training on liver fat accumulation and estrogen receptor alpha expression in intact and ovariectomized rats with or without estrogen replacement treatment. Eur. J. Appl. Physiol. 2010, 109(5):879-886.
28. Hemmings B.A., Restuccia D.F. PI3K-PKB/Akt pathway. Cold Spring Harb. Perspect. Biol. 2012, 4(9):a011189.
29. Hewitt K.N., Pratis K., Jones M.E., Simpson E.R. Estrogen replacement reverses the hepatic steatosis phenotype in the male aromatase knockout mouse. Endocrinology 2004, 145(4):1842-1848.
30. Huang A., Kaley G. Gender-specific regulation of cardiovascular function: estrogen as key player. Microcirculation 2004, 11(1):9-38.
31. +/K(+)-ATPase from intracellular compartments to the plasma membrane in mammalian skeletal muscle. J. Biol. Chem. 1992, 267(8):5040-5043.
32. Hunter S.J., Garvey W.T. Insulin action and insulin resistance: diseases involving defects in insulin receptors, signal transduction, and the glucose transport effector system. Am. J. Med. 1998, 105(4):331-345.
33. Iannello, S., Campione, R., Volpicelli, G., Prestipino, M., Belfiore, F., 1994. Na, K-adenosine triphosphatase in mouse and human obesity and diabetes, as related to insulin, NEFA and hypertension. Diabetologia, Catania, Italy, p. A133.
34. Iannello S., Milazzo P., Belfiore F. Animal and human tissue Na, K-ATPase in normal and insulin-resistant states: regulation, behaviour and interpretative hypothesis on NEFA effects. Obes. Rev. 2007, 8(3):231-251.
35. Iannello S., Milazzo P., Belfiore F. Animal and human tissue Na, K-ATPase in obesity and diabetes: a new proposed enzyme regulation. Am. J. Med. Sci. 2007, 333(1):1-9.
36. Isenovic E., LaPointe M.C. Role of Ca(2+)-independent phospholipase A(2) in the regulation of inducible nitric oxide synthase in cardiac myocytes. Hypertension 2000, 35(1 Pt 2):249-254.
37. Isenovic, E.R., Sha, Q., Milivojevic, N.M., Sowers, J.R., 2002. Ang II inhibits E2-induced nitric oxide production and gene expression of the catalytic subunit of the sodium pump in VSMC. In: Proceedings of 62nd Scientific Sessions, Supplement 2, Diabetes, Moscone Center, San Francisco.
38. Isenovic E.R., Divald A., Milivojevic N., Grgurevic T., Fisher S.E., Sowers J.R. Interactive effects of insulin-like growth factor-1 and beta-estradiol on endothelial nitric oxide synthase activity in rat aortic endothelial cells. Metabolism 2003, 52(4):482-487.
39. + pump involves the phosphatidylinositol-3 kinase and p42/44 mitogen-activated protein kinase signaling pathways in vascular smooth muscle cells. Endocrinology 2004, 145(3):1151-1160.
40. +, K(+)-ATPase activity via PI3K/Akt pathway in vascular smooth muscle cells. Int. J. Mol. Med. 2004, 13(6):915-922.
41. Isenovic E.R., Fretaud M., Koricanac G., Sudar E., Velebit J., Dobutovic B., Marche P. Insulin regulation of proliferation involves activation of AKT and ERK1/2 signaling pathways in vascular smooth muscle cells. Exp. Clin. Endocrinol. Diabetes 2009, 117(5):214-219.
42. Jelenik T., Roden M. How estrogens prevent from lipid-induced insulin resistance. Endocrinology 2013, 154(3):989-992.
43. Kaplan JH. Biochemistry of Na, K-ATPase. Annu. Rev. Biochem. 2002, 71511-71535.
44. Katz A.I., Epstein F.H. The role of sodium-potassium-activated adenosine triphosphatase in the reabsorption of sodium by the kidney. J. Clin. Invest. 1967, 46(12):1999-2011.
45. Kelly M.J., Levin E.R. Rapid actions of plasma membrane estrogen receptors. Trends Endocrinol. Metab. 2001, 12(4):152-156.
46. Knowlton A.A., Lee A.R. Estrogen and the cardiovascular system. Pharmacol. Ther. 2012, 135(1):54-70.
47. Koricanac G., Tepavcevic S., Zakula Z., Milosavljevic T., Stojiljkovic M., Isenovic E.R. Interference between insulin and estradiol signaling pathways in the regulation of cardiac eNOS and Na(+)/K(+)-ATPase. Eur. J. Pharmacol. 2011, 655(1-3):23-30.
48. Kumagai S., Holmang A., Bjorntorp P. The effects of oestrogen and progesterone on insulin sensitivity in female rats. Acta Physiol. Scand. 1993, 149(1):91-97.
49. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227(5259):680-685.
50. Laube M., Kuppers E., Thome U.H. Modulation of sodium transport in alveolar epithelial cells by estradiol and progesterone. Pediatr. Res. 2011, 69(3):200-205.
51. Levin E.R. Integration of the extranuclear and nuclear actions of estrogen. Mol. Endocrinol. 2005, 19(8):1951-1959.
52. Lichtstein D., Steinitz M., Gati I., Samuelov S., Deutsch J., Orly J. Biosynthesis of digitalis-like compounds in rat adrenal cells: hydroxycholesterol as possible precursor. Life Sci. 1998, 62(23):2109-2126.
53. 2+-ATPase and carbonic anhydrase iv in H9C2 cells. Clin. Exp. Pharmacol. Physiol. 2007, 34(10):998-1004.
54. Liu C., Bai Y., Chen Y., Wang Y., Sottejeau Y., Liu L., Li X., Lingrel J.B., Malhotra D., Cooper C.J., et al. Reduction of Na/K-ATPase potentiates marinobufagenin-induced cardiac dysfunction and myocyte apoptosis. J. Biol. Chem. 2012, 287(20):16390-16398.
55. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193(1):265-275.
56. Luiken J.J., Koonen D.P., Willems J., Zorzano A., Becker C., Fischer Y., Tandon N.N., Van Der Vusse G.J., Bonen A., Glatz J.F. Insulin stimulates long-chain fatty acid utilization by rat cardiac myocytes through cellular redistribution of FAT/CD36. Diabetes 2002, 51(10):3113-3119.
57. Manning B.D., Cantley L.C. AKT/PKB signaling: navigating downstream. Cell 2007, 129(7):1261-1274.
58. Marín-García J. Cardiac function in heart failure: the role of calcium cycling. Heart Failure 2010, 15-21. Springer.
59. Muniyappa R., Sowers J.R. Role of insulin resistance in endothelial dysfunction. Rev. Endocr. Metab. Disord. 2013, 14(1):5-12.
60. Murphy E. Estrogen signaling and cardiovascular disease. Circ. Res. 2011, 109(6):687-696.
61. Nadal-Ginard B., Kajstura J., Leri A., Anversa P. Myocyte death, growth, and regeneration in cardiac hypertrophy and failure. Circ. Res. 2003, 92(2):139-150.
62. Niba E.T., Nagaya H., Kanno T., Tsuchiya A., Gotoh A., Tabata C., Kuribayashi K., Nakano T., Nishizaki T. Crosstalk between PI3Kinase/PDK1/Akt/Rac1 and Ras/Raf/MEK/ERK Pathways Downstream PDGF Receptor. Cell. Physiol. Biochem. 2013, 31(6):905-913.
63. Nilsson S., Gustafsson J.A. Estrogen receptor action. Crit. Rev. Eukaryot. Gene Expr. 2002, 12(4):237-257.
64. Nilsson S., Makela S., Treuter E., Tujague M., Thomsen J., Andersson G., Enmark E., Pettersson K., Warner M., Gustafsson J.A. Mechanisms of estrogen action. Physiol. Rev. 2001, 81(4):1535-1565.
65. Norgaard A., Bagger J.P., Bjerregaard P., Baandrup U., Kjeldsen K., Thomsen P.E. Relation of left ventricular function and Na, K-pump concentration in suspected idiopathic dilated cardiomyopathy. Am. J. Cardiol. 1988, 61(15):1312-1315.
66. +-ATPase and their relevance to cardiovascular disease. J. Endocrinol. 2013, 218(3):R13-R23.
67. Obradovic M., Sudar E., Zafirovic S., Stanimirovic J., Labudovic-Borovic M., Isenovic E.R. Estradiol in vivo induces changes in cardiomyocytes size in obese rats. Angiology 2013.
68. Ohshiro K., Rayala S.K., Williams M.D., Kumar R., El-Naggar A.K. Biological role of estrogen receptor beta in salivary gland adenocarcinoma cells. Clin. Cancer Res. 2006, 12(20 Pt 1):5994-5999.
69. Olson A.K., Ledee D., Iwamoto K., Kajimoto M., O'Kelly Priddy C., Isern N Portman M.A. C-Myc induced compensated cardiac hypertrophy increases free fatty acid utilization for the citric acid cycle. J. Mol. Cell. Cardiol. 2013, 55156-55164.
70. Palacios J., Marusic E.T., Lopez N.C., Gonzalez M., Michea L. Estradiol-induced expression of N(+)-K(+)-ATPase catalytic isoforms in rat arteries: gender differences in activity mediated by nitric oxide donors. Am. J. Physiol. Heart Circ. Physiol. 2004, 286(5). H1793-800.
71. Patten R.D., Pourati I., Aronovitz M.J., Baur J., Celestin F., Chen X., Michael A., Haq S., Nuedling S., Grohe C., et al. 17beta-estradiol reduces cardiomyocyte apoptosis in vivo and in vitro via activation of phospho-inositide-3 kinase/Akt signaling. Circ. Res. 2004, 95(7):692-699.
72. Pedram A., Razandi M., O'Mahony F., Lubahn D., Levin E.R. Estrogen receptor-beta prevents cardiac fibrosis. Mol. Endocrinol. 2010, 24(11):2152-2165.
73. Pudek M.R., Seccombe D.W., Jacobson B.E., Whitfield M.F. Seven different digoxin immunoassay kits compared with respect to interference by a digoxin-like immunoreactive substance in serum from premature and full-term infants. Clin. Chem. 1983, 29(11):1972-1974.
74. Rathore S.S., Curtis J.P., Wang Y., Bristow M.R., Krumholz H.M. Association of serum digoxin concentration and outcomes in patients with heart failure. JAMA 2003, 289(7):871-878.
75. Ren J., Hintz K.K., Roughead Z.K., Duan J., Colligan P.B., Ren B.H., Lee K.J., Zeng H. Impact of estrogen replacement on ventricular myocyte contractile function and protein kinase B/Akt activation. Am. J. Physiol. Heart Circ. Physiol. 2003, 284(5). H1800-7.
76. Resanovic I., Rizzo M., Zafirovic S., Bjelogrlic P., Perovic M., Savic K., Patti A.M., Isenovic R.E. Anti-atherogenic effects of 17beta-estradiol. Horm. Metab. Res 2013.
77. Sarbassov D.D., Guertin D.A., Ali S.M., Sabatini D.M. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 2005, 307(5712):1098-1101.
78. Schlegel A., Wang C., Pestell R.G., Lisanti M.P. Ligand-independent activation of oestrogen receptor alpha by caveolin-1. Biochem J. 2001, 359(Pt 1):203-210.
79. Schwinger R.H., Bundgaard H., Muller-Ehmsen J., Kjeldsen K. The Na, K-ATPase in the failing human heart. Cardiovasc. Res. 2003, 57(4):913-920.
80. Shamraj O.I., Grupp I.L., Grupp G., Melvin D., Gradoux N., Kremers W., Lingrel J.B., De Pover A. Characterisation of Na/K-ATPase, its isoforms, and the inotropic response to ouabain in isolated failing human hearts. Cardiovasc. Res. 1993, 27(12):2229-2237.
81. Simoncini T., Hafezi-Moghadam A., Brazil D.P., Ley K., Chin W.W., Liao J.K. Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase. Nature 2000, 407(6803):538-541.
82. Simoncini T., Fornari L., Mannella P., Varone G., Caruso A., Liao J.K., Genazzani A.R. Novel non-transcriptional mechanisms for estrogen receptor signaling in the cardiovascular system. Interaction of estrogen receptor alpha with phosphatidylinositol 3-OH kinase. Steroids 2002, 67(12):935-939.
83. Slinker B.K., Stephens R.L., Fisher S.A., Yang Q. Immediate-early gene responses to different cardiac loads in the ejecting rabbit left ventricle. J. Mol. Cell. Cardiol. 1996, 28(7):1565-1574.
84. Sovershaev M.A., Egorina E.M., Andreasen T.V., Jonassen A.K., Ytrehus K. Preconditioning by 17beta-estradiol in isolated rat heart depends on PI3-K/PKB pathway, PKC, and ROS. Am. J. Physiol. Heart Circ. Physiol. 2006, 291(4). H1554-62.
85. Sowers J.R., Sowers P.S., Peuler J.D. Role of insulin resistance and hyperinsulinemia in development of hypertension and atherosclerosis. J. Lab. Clin. Med. 1994, 123(5):647-652.
86. Stubbins R.E., Najjar K., Holcomb V.B., Hong J., Nunez N.P. Oestrogen alters adipocyte biology and protects female mice from adipocyte inflammation and insulin resistance. Diabetes Obes. Metab. 2012, 14(1):58-66.
87. Sudar E., Velebit J., Gluvic Z., Zakula Z., Lazic E., Vuksanovic-Topic L., Putnikovic B., Neskovic A., Isenovic E.R. Hypothetical mechanism of sodium pump regulation by estradiol under primary hypertension. J. Theor. Biol. 2008, 251(4):584-592.
88. Sudar E., Dobutovic D., Milosavljevic T., Putnikovic B., Gluvic Z., Isenovic E. Interactive effects of insulin and β-estradiol on protein kinase B phosphorylation in adult rat cardiomyocytes. Acta Chim. Slov. 2009, 56723-56728.
89. Taras M.J., Greenberg A.E., Hoak R.D., Rand M.C. Standard Methods for the Examination of Water and Wastewater 1971, DC American Public Health Association, Washington.
90. Therien A.G., Blostein R. Mechanisms of sodium pump regulation. Am. J. Physiol. Cell Physiol. 2000, 279(3):C541-C566.
91. +-ATPase forms a functional signaling complex. Mol. Biol. Cell 2006, 17(1):317-326.
92. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 1979, 76(9):4350-4354.
93. Treasure J.L., Ploth D.W., Treasure T. Measurement of potassium concentration on-line with an ion-specific electrode during hemodialysis. Miner. Electrolyte Metab. 1986, 12(3):161-164.
94. van Eickels M., Grohe C., Cleutjens J.P., Janssen B.J., Wellens H.J., Doevendans P.A. 17beta-estradiol attenuates the development of pressure-overload hypertrophy. Circulation 2001, 104(12):1419-1423.
95. van Son J.A., Smedts F., de Wilde P.C., Pijls N.H., Wong-Alcala L., Kubat K., Tavilla G., Lacquet L.K. Histological study of the internal mammary artery with emphasis on its suitability as a coronary artery bypass graft. Ann. Thorac. Surg. 1993, 55(1):106-113.
96. Voloshenyuk T.G., Gardner J.D. Estrogen improves TIMP-MMP balance and collagen distribution in volume-overloaded hearts of ovariectomized females. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 299(2):R683-R693.
97. Wagner J.D., Thomas M.J., Williams J.K., Zhang L., Greaves K.A., Cefalu W.T. Insulin sensitivity and cardiovascular risk factors in ovariectomized monkeys with estradiol alone or combined with nomegestrol acetate. J. Clin. Endocrinol. Metab. 1998, 83(3):896-901.
98. Worth HG. A comparison of the measurement of sodium and potassium by flame photometry and ion-selective electrode. Ann. Clin. Biochem. 1985, 22(Pt 4):343-350.
99. Wu Q., Zhao Z., Sun H., Hao Y.L., Yan C.D., Gu S.L. Oestrogen changed cardiomyocyte contraction and beta-adrenoceptor expression in rat hearts subjected to ischaemia-reperfusion. Exp. Physiol. 2008, 93(9):1034-1043.
100. Xiao G., Mao S., Baumgarten G., Serrano J., Jordan M.C., Roos K.P., Fishbein M.C., MacLellan W.R. Inducible activation of c-Myc in adult myocardium in vivo provokes cardiac myocyte hypertrophy and reactivation of DNA synthesis. Circ. Res. 2001, 89(12):1122-1129.
101. Yamamoto S., Akera T., Brody T.M. Positive inotropic action of digoxigenin and sodium pump inhibition: effects of enhanced sodium influx. J. Pharmacol. Exp. Ther. 1980, 213(1):105-109.
102. Zahler R., Gilmore-Hebert M., Sun W., Benz E.J. Na, K-ATPase isoform gene expression in normal and hypertrophied dog heart. Basic Res. Cardiol. 1996, 91(3):256-266.
103. Zhu L., Brown W.C., Cai Q., Krust A., Chambon P., McGuinness O.P., Stafford J.M. Estrogen treatment after ovariectomy protects against fatty liver and may improve pathway-selective insulin resistance. Diabetes 2013, 62(2):424-434.